Functional traits provide new insight into recovery and succession at deep-sea hydrothermal vents

© The Author(s), 2021. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Dykman, L. N., Beaulieu, S. E., Mills, S. W., Solow, A. R., & Mullineaux, L. S. Functional traits provide new insight into recovery and succession at deep-sea hydrothermal vents. Ecology, 102(8), (2021): e03418, https://doi.org/10.1002/ecy.3418.Investigation of communities in extreme environments with unique conditions has the potential to broaden or challenge existing theory as to how biological communities assemble and change through succession. Deep-sea hydrothermal vent ecosystems have strong, parallel gradients of nutrients and environmental stress, and present unusual conditions in early succession, in that both nutrient availability and stressors are high. We analyzed the succession of the invertebrate community at 9°50′ N on the East Pacific Rise for 11 yr following an eruption in 2006 in order to test successional theories developed in other ecosystems. We focused on functional traits including body size, external protection, provision of habitat (foundation species), and trophic mode to understand how the unique nutritional and stress conditions influence community composition. In contrast to established theory, large, fast-growing, structure-forming organisms colonized rapidly at vents, while small, asexually reproducing organisms were not abundant until later in succession. Species in early succession had high external protection, as expected in the harsh thermal and chemical conditions after the eruption. Changes in traits related to feeding ecology and dispersal potential over succession agreed with expectations from other ecosystems. We also tracked functional diversity metrics over time to see how they compared to species diversity. While species diversity peaked at 8 yr post-eruption, functional diversity was continuing to increase at 11 yr. Our results indicate that deep-sea hydrothermal vents have distinct successional dynamics due to the high stress and high nutrient conditions in early succession. These findings highlight the importance of extending theory to new systems and considering function to allow comparison between ecosystems with different species and environmental conditions.Funding for L. Dykman, L. Mullineaux, and S. Beaulieu was provided by NSF OCE-1829773. The Synthesis Centre of the German Centre for Integrative Biodiversity Research (sDiv) funded the sFDvent working group and database

Marine Parasites in Island-like Disturbed Habitats

Parasites are taxonomically and functionally diverse members of biological communities, and can play key roles in species interactions, community structure, and ecosystem functioning. For their reliance on host species, parasites are theorized to be particularly sensitive to disturbances that alter host diversity and abundance, especially in isolated habitats, which present challenges to introduction and establishment. In this thesis, I investigate habitat isolation and disturbance as drivers of parasite diversity, with an emphasis on parasite life history strategies related to colonization and persistence. I focus on an island-like, frequently disturbed habitat, deep sea hydrothermal vents at 9∘ 50’N on the East Pacific Rise, to explore the boundaries of parasite persistence in an extreme environment. First, I analyze recovery in the vent community for 11 years after a catastrophic eruption in 2006 to test successional hypotheses in a new setting with distinct fauna and a chemosynthesis-based food web. Second, I compare parasite diversity at isolated, disturbed vents to marine ecosystems that are similarly isolated but undisturbed (atoll sandflat) and both well connected and undisturbed (kelp forest). Overall, parasite diversity within host species was not significantly lower at vents, but the vent community had manyfewer parasite species because there arefew vertebrate predator species (fish). Parasites with indirect (multi-host) life cycles were relatively diverse in the disturbed environment, which contradicts expectation based on theory. To explore this further, I investigate the three-host life cycles of trematodes at vents, which was the most diverse and abundant parasite taxon. All life stages of the trematode life cycle were discovered in ventfauna and several taxa were traced across multiple life stages via morphology and genetics. Finally, I use a computational model to investigate how different parasite strategies (colonization capability and impact on hosts) contribute to parasite success under a range of disturbance conditions in island habitats. Parasites that reduce host reproduction reached higher densities than parasites that cause mortality across all disturbance frequencies explored, and disturbance facilitated the evolution of more virulent parasites. These studies demonstrate that life history traits and the ability to adapt allow diverse parasite taxa to persist in isolated, ephemeral environments.Ph.D

Effect of habitat cues on the swimming behavior of pre-competent Lacuna vincta larvae from Friday Harbor, WA, USA

Swimming behavior in planktonic larvae has been suggested to affect their dispersal and recruitment. Behavioral regulation of vertical distribution can affect the extent to which larvae may accumulate in or escape from vertically sheared flows or fronts. Competent larvae of many invertebrate species are known to respond to various settlement cues in the environment by regulating their behavior in order to facilitate settling in suitable habitats. The behavioral responses of pre-competent larvae to cues from the adult habitat could have implications for retention, however such responses have not been investigated. In this project we have studied the swimming behavior in pre-competent larvae from the gastropod Lacuna vincta in the laboratory with the objective of determining whether behavioral changes in response to potential settlement cues are present in larvae at that earlier developmental stage. Potential settlement cues included in this study are eelgrass (Zostera marina), the kelp Agarum fimbriatum, and adult L. vincta, in addition to a control of filtered seawater. Pre-competent L.vincta larvae were recorded swimming in water columns containing water in which these various cues had been soaked, and their behaviors were compared across treatments. Videos were analyzed for mean upward swimming speed, mean swimming speed along the path of travel, mean oscillatory speed, and mean axial speed for each treatment. For all metrics, there were no significant differences between all four treatments and the control. The sample size of larvae was consistently low in the kelp cue as larvae remained on the bottom of the column, possibly due to high viscosity of that cue water. Our results indicated no response to adult habitat cues when larvae are pre-competent

Effects of hypoxic layers on the swimming behavior of Lacuna vincta larvae from Friday Harbor, WA, USA

Hypoxia has the potential to influence marine organism function at many stages in the life cycle. Most studies on benthic invertebrates have focused on adult animals, but it is important to consider impacts on larvae, as they will have consequences for survival and recruitment of benthic populations. We sought to determine whether hypoxia alters the swimming behavior of Lacuna vincta larvae, and whether larvae are able to recognize and avoid hypoxic layers. We used video recording to compare larval behavior in stratified water columns with an upper layer with normoxic oxygen levels (~85% saturation, ~7.5 mg/L) and a lower layer with hypoxic oxygen levels (~13% saturation, ~1 mg/L), to behavior in similarly stratified columns where both upper and lower layers were normoxic (~85% saturation, ~7.5 mg/L). The vast majority of L. vincta larvae recorded in the videos were concentrated at the surface in our experiments. Trends among the small fraction of larvae not clustered at the top 20 mm of the columns showed: (1) slower swimming speed along the path of travel in the hypoxic lower layer than the control lower layer, (2) slower downward velocity in the hypoxic columns than the control columns, (3) faster upward velocity in the hypoxic columns than the control columns, (4) the presence of larvae on the very bottom of the control columns versus a near absence of larvae at the bottom of the hypoxic treatment columns, and (5) a slightly higher fraction of time spent in the lower layer in the control columns. The small magnitudes of these differences may be due to the small number of larvae that traveled down below the surface in the columns in all treatments, or may indicate a relatively low sensitivity to hypoxia in this species. As global climate change continues and coastal hypoxia increases in frequency and severity, it is crucial to improve our understanding of the impacts of hypoxia across ontogenetic stages of marine invertebrates, so as to understand the implications for survival, recruitment, and population resilience. Results of this study demonstrate that upswimming tendencies may reduce encounters of L.vincta larvae with hypoxia, that larvae alter swimming behaviors in response to hypoxia, and that the observed behavioral changes appear generally consistent with a weak ability to escape or avoid hypoxia layers

Functional traits of colonists collected from colonization surfaces at the East Pacific Rise (EPR) deep-sea vents from 1998-2017

Dataset: EPR vent colonists functional traitsFunctional traits of colonists collected from colonization surfaces at the East Pacific Rise (EPR) deep-sea vents (1998-2017) (Dykman et al., 2021). A dataset of trait modality assignments for 8 functional traits of 58 invertebrate species or higher taxa (when species ID was uncertain) collected from colonization surfaces deployed at hydrothermal vents at 9° 50’N on the East Pacific Rise. For a complete list of measurements, refer to the full dataset description in the supplemental file 'Dataset_description.pdf'. The most current version of this dataset is available at: https://www.bco-dmo.org/dataset/844993NSF Division of Ocean Sciences (NSF OCE) OCE-182977